Eur. J. Entomol. 120: 170-181, 2023 | DOI: 10.14411/eje.2023.022

An overview of the pollination interactions between the ginger family (Zingiberaceae) and insects in AsiaReview

Suganthi APPALASAMY ORCID...1, 2, Nivaarani ARUMUGAM ORCID...2, Visweswara Rao PASUPULETI ORCID...3, 4, Sreeramanan SUBRAMANIAM ORCID...5, 6, Jayaraj Vijaya KUMARAN ORCID...2, Maryana Mohamad NOR ORCID...1, 7, Mohammed Abdus SALAM ORCID...8
1 Institute of Food Security and Sustainable Agriculture (IFSSA), Universiti Malaysia Kelantan (UMK), Jeli Campus, 17600 Jeli, Kelantan, Malaysia; e-mails: suganthi.a@umk.edu.my, maryana.mn@umk.edu.my
2 Faculty of Earth Science, Universiti Malaysia Kelantan (UMK), Jeli Campus, 17600 Jeli, Kelantan, Malaysia; e-mails: niva035@gmail.com, jayaraj@umk.edu.my
3 Centre for International Relations and Research Collaborations, REVA University, Rukmini Knowledge Park, Kattigenahalli, Yelahanka, Bangalore 560064, Karnataka, India; e-mail: visuthebiotech@gmail.com
4 School of Biosciences, Faculty of Health and Medical Sciences, Taylor's University, 1, Jalan Taylor's, 47500 Subang Jaya, Selangor, Malaysia
5 School of Biological Sciences, Universiti Sains Malaysia (USM), 11800, Gelugor, Pulau Pinang, Malaysia; e-mail: sreeramanan@gmail.com
6 Chemical Centre Biology (CCB), Universiti Sains Malaysia (USM), 11900 Bayan Lepas, Pulau Pinang, Malaysia
7 Faculty of Agro Based Industry, Universiti Malaysia Kelantan (UMK) Jeli Campus, 17600 Jeli, Kelantan, Malaysia
8 Department of Environmental Science and Disaster Management, Noakhali Science and Technology University, Noakhali, Bangladesh; e-mail: masalam.esdm@nstu.edu.bd

The plant-biotic pollinator interaction is crucial for the survival of both organisms. Insects are recognised as effective biotic pollinators. As there are few specific studies on the pollination of angiosperms, the emphasis of this review is on understanding the pollination process by reviewing the knowledge of the ginger-insect pollinator interaction in Asia. Currently the plant-pollinator interaction of only 5% of Asian species of Zingiberaceae is evaluated. Previous studies indicate that bees, such as, halictid and blue-banded bees are, among the many floral vistors, the most important pollinators of ginger plants in Asia. Knowledge of non-bee pollinators is still scarce. In order to obtain a more detailed understanding of the interrelationship of the pollinators of ginger plants with the morphology of their flowers, floral scent and geographical factors, further research is needed.

Keywords: Plant, flower, floral visitor, mutualism

Received: September 1, 2022; Revised: May 9, 2023; Accepted: May 9, 2023; Published online: June 1, 2023  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
APPALASAMY, S., ARUMUGAM, N., PASUPULETI, V.R., SUBRAMANIAM, S., KUMARAN, J.V., NOR, M.M., & SALAM, M.A. (2023). An overview of the pollination interactions between the ginger family (Zingiberaceae) and insects in Asia. EJE, 120, Article 170-181. https://doi.org/10.14411/eje.2023.022
Share...
Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)
    • Open full article

    References

    1. Abrol D.P., Gorka A.K., Ansari M.J., Al-Ghamdi A. & Al-Kahtani S. 2019: Impact of insect pollinators on yield and fruit quality of strawberry. - Saudi J. Biol. Sci. 26: 527-530. Go to original source...
    2. Alanís-Méndez J.L., Ortiz-Santos L.d.C., Chamorro-Florescano I.A., Pech-Canché J.M. & Limón F. 2019: Pollinators and floral visitors of two orchids in a protected natural area in Tuxpan, Veracruz. - Ecosist. Recurs. Agropecuar. 6: 361-368. Go to original source...
    3. Alves-dos-Santos I., Silva C.I.d., Pinheiro M. & Kleinert A. d.M.P. 2016: Quando um visitante floral é um polinizador? - Rodriguésia 67: 295-307. Go to original source...
    4. Angiosperm Phylogeny Group (APG II) 2003: An update of the angiosperm phylogeny group classification for the orders and families of flowering plants: APG II. - Bot. J. Linn. Soc. 141: 399-436. Go to original source...
    5. Appalasamy S. & Arumugam N. 2020: Four new records of Zingiberaceae in Gunung Telapak Burok, Berembun Forest Reserve (Fr), Negeri Sembilan. - IOP Conf. Ser.: Earth Environ. Sci. 596: 012059, 6 pp. Go to original source...
    6. Appalasamy S., Arumugam N., Boon J.G. & Aweng E.R. 2019: A short note on wild gingers (Zingiberaceae) in Pulau Pangkor, Perak, peninsular Malaysia. - Malaysian Forester 82: 159-162.
    7. Appalasamy S., Arumugam N., Lam Y. & Nur Azizun R. 2020a: Wild gingers (Zingiberaceae) at Sungai Kangkawat, Imbak canyon conservation area (ICCA), Sabah. - J. Trop. Biol. Conserv. 17: 97-103. Go to original source...
    8. Appalasamy S., Rathamanalan S., Arsogah S., Harni S., Sam K.K., Amaludin N.A., Geng B.J., Kumaran J.V., Arumugam N. & Subramaniam S. 2020b: Gingers species diversity and distribution along a natural trail of Lojing highlands, Kelantan. - IOP Conf. Ser.: Earth Environ. Sci. 549: 012036, 5 pp. Go to original source...
    9. Appalasamy S., Arumugam N., Zamri N.S.A., Fadhlina A., Kumaran J.V. & Subramaniam S. 2022: First report on wild ginger (Family: Zingiberaceae) species composition with new records in limestone forests of Kelantan, Peninsular Malaysia. - Trop. Life Sci. Res. 33: 33-46. Go to original source...
    10. Arumugam N., Zamri N.S., Kumaran J.V., Nor M.M., Subramaniam S. & Appalasamy S. 2022: First report on pollinating behavior of the small carpenter bee Ceratina ridleyi Cockerell (Hymenoptera, Apidae) in Globba leucantha var. bicolor Holttum (Zingiberaceae). - J. Hymenopt. Res. 90: 173-183. Go to original source...
    11. Aswani K.K. & Sabu M.M. 2018: Reproductive biology of dancing girl ginger, Globba schomburgkii (Zingiberaceaeae). - Int. J. Plant Reprod. Biol. 10: 184-188.
    12. Aswani K., Sabu M. & Smisha K.P. 2013: Reproductive biology of Etlingera elatior (Jack.) R. M. Sm. ornamental torch ginger. - Int. J. Plant Anim. Environ. Sci. 3: 75-80.
    13. Ayasse M., Stökl J. & Francke W. 2011: Chemical ecology and pollinator-driven speciation in sexually deceptive orchids. - Phytochemistry 72: 1667-1677. Go to original source...
    14. Baqi A., Lim V.C., Yazid H., Khan F.A.A., Lian C.J., Nelson B.R., Seelan J.S.S., Appalasamy S., Mokhtar S.I. & Kumaran J.V. 2022: A review of durian plant-bat pollinator interactions. - J. Plant Interact. 17: 105-126. Go to original source...
    15. Binghong X., Chunyan L., Xinlan X., Bo C., Caixia A., Shiquan L., Xiongyao H., Jian C., Lian L. & Li T. 2018: Studies on collection breeding and application of Zingiberaceae plants wild resources in China. - J. Plant Sci. 6: 179-184.
    16. Bond W.J. 1994: Do mutualisms matter? Assessing the impact of pollinator and disperser disruption on plant extinction. - Phil. Trans. R. Soc. Lond. (B) 344: 83-90. Go to original source...
    17. Brothers A.N. & Atwell J.W. 2014: The role of pollinator-mediated selection in the divergence of floral traits between two closely related plant species. - Int. J. Plant Sci. 175: 287-295. Go to original source...
    18. Buchholz S. & Kowarik I. 2019: Urbanisation modulates plant-pollinator interactions in invasive vs. native plant species. - Sci. Rep. 9: 6375, 9 pp. Go to original source...
    19. Bumrungsri S., Harbit A., Benzie C. & Carmouche K. 2008: The pollination ecology of two species of Parkia (Mimosaceae) in southern Thailand. - J. Trop. Ecol. 24: 467-447. Go to original source...
    20. Campbell N.A. & Reece J.B. 2008: Biology. 8th ed. Pearson Benjamin Cummings, Frenchs Forest, N.S.W., 1267 pp.
    21. Chautá-Mellizo A., Campbell S.A., Bonilla M.A., Thaler J.S. & Poveda K. 2012: Effects of natural and artificial pollination on fruit and offspring quality. - Basic Appl. Ecol. 13: 524-532. Go to original source...
    22. Chongkraijak W., Ngamnriabsakul C. & Poulsen A.D. 2013: Morphological diversity and distribution of Etlingera littoralis (König) Giseke (Zingiberaceae) in Southern Thailand. - Walailak J. Sci. Tech. 10: 643-656.
    23. Choon S.Y. & Ding P. 2016: Growth stages of torch ginger (Etlingera elatior) plant. - Sains Malaysiana 45: 507-515.
    24. Classen R. 1987: Morphological adaptations for bird pollination in Nicolaia elatior (Jack) Horan (Zingiberaceae). - Garden's Bull. (Singapore) 40: 37-42.
    25. Convention on Biological Diversity 2018: Review of Pollinators and Pollination Relevant to the Conservation and Sustainable Use of Biodiversity in All Ecosystems, Beyond Their Role in Agriculture and Food Production. Convention's Subsidiary Body on Scientific, Technical and Technological Advice (SBSTTA). URL: https://www.cbd.int/agro/peer_review_pollinators.pdf
    26. Criley R.A. 1995: Propagation of Zingiberaceae and Heliconiaceae. - Rev. Brss. Hort. Orn. Campinas 1: 14-21. Go to original source...
    27. Darwin C.R. 1862: On the various contrivances by which british and foreign orchids are fertilized by insects, and on the good effects of intercrossing. - Ann. Mag. Nat. Hist. 10: 384-388. Go to original source...
    28. Davies T.J., Barraclough T.G., Chase M.W., Soltis P.S., Soltis D.E. & Savolainen V. 2004: Darwin's abominable mystery: Insights from a supertree of the angiosperms. - Proc. Natn. Acad. Sci. 101: 1904-1909. Go to original source...
    29. de Merxem D.G., Borremans B., de Jäger M.L., Johnson T., Jooste M., Ros P., Zenni R.D., Ellis A.G. & Anderson B. 2009: The importance of flower visitors not predicted by floral syndromes. - Sth Afr. J. Bot. 75: 660-667. Go to original source...
    30. Denisow B. 2009: Pollen production, flowering and insect visits on Euphorbia cyparissias L. and Euphorbia virgultosa Klok. - J. Apicult. Res. 48: 50-59. Go to original source...
    31. Denisow B., Strza³kowska-Abramek M., Bo¿ek M. & Je¿ak A. 2014: Ornamental representatives of the genus Centaurea L. as a pollen source for bee friendly gardens. - J. Apicult. Sci. 58: 49-58. Go to original source...
    32. Deschepper P., Brys R. & Jacquemyn H. 2018: The impact of flower morphology and pollinator community composition on pollen transfer in the distylous Primula veris. - Bot. J. Linn. Soc. 186: 414-424. Go to original source...
    33. Dictionary.com 2023: -phily. URL: https://www.dictionary.com/browse/-phily (last accessed 22 Mar 2023).
    34. Diego C.E.N., Stewart A.B. & Bumrungsri S. 2021: Pollinators necessary for the reproductive success of critically endangered mangrove, Sonneratia griffithii. - Aquatic Bot. 169: 103340, 5 pp. Go to original source...
    35. Dobson H.E.M. 2006: Relationship between floral fragrance composition and type of pollinator. In Dudareva N. & Pichersky E. (eds): Biology of Floral Scent. CRC Press, Boca Raton, pp. 147-198. Go to original source...
    36. Doyle T., Hawkes W.L.S., Massy R., Powney G.D., Menz M.H.M. & Wotton K.R. 2020: Pollination by hoverflies in the Anthropocene. - Proc. R. Soc. (B) 287: 20200508, 9 pp. Go to original source...
    37. Eeraerts M., Vanderhaegen R., Smagghe G. & Meeus I. 2019: Pollination efficiency and foraging behaviour of honey bees and non-Apis bees to sweet cherry. - Agric. Forest Entomol. 22: 75-82. Go to original source...
    38. Fenster C.B., Armbruster W.S., Wilson P., Dudash M.R. & Thomson J.D. 2004: Pollination syndromes and floral specialization. - Ann. Rev. Ecol. Evol. Syst. 35: 375-403. Go to original source...
    39. Field D.L., Pickup M. & Barrett S.C.H. 2012: The influence of pollination intensity on fertilization success, progeny sex ratio, and fitness in a wind-pollinated, dioecious plant. - Int. J. Plant Sci. 173: 184-191. Go to original source...
    40. Fumero-Cabán J.J. & Meléndez-Ackerman E.J. 2007: Relative pollination effectiveness of floral visitors of Pitcairnia angustifolia (Bromeliaceae). - Am. J. Bot. 94: 419-424. Go to original source...
    41. Gao J.-Y., Zhang L., Deng X.-B., Ren P.-Y., Kong J.-J. & Li Q.-J. 2004: The floral biology of Curcumorpha longiflora (Zingiberaceae): a ginger with two-day flowers. - Am. J. Bot. 91: 289-293. Go to original source...
    42. Hernández-Villa V., Vibrans H., Uscanga-Mortera E. & Aguirre-Jaimes A. 2020: Floral visitors and pollinator dependence are related to floral display size and plant height in native weeds of central Mexico. - Flora 262: 151505, 9 pp. Go to original source...
    43. Hingston A.B. & Mc Quillan P.B. 2000: Are pollination syndromes useful predictors of floral visitors in Tasmania? - Austral. Ecol. 25: 600-609. Go to original source...
    44. Huang Z.Y. & Giray T. 2012: Factors affecting pollinators and pollination. - Psyche 2012: 302409, 3 pp. Go to original source...
    45. Inouye D.W. 2007: Pollinators, role of. In Levin S.A. (ed.): Encyclopedia of Biodiversity. Vol. 6. Elsevier, Amsterdam, pp. 140-146. Go to original source...
    46. Ippolito A. & Armstrong J.E. 1993: Floral biology of Hornstedtia scottiana (Zingiberaceae) in a lowland rain forest of Australia. - Biotropica 25: 281-289. Go to original source...
    47. Izlamira R., Appalasamy S., Nivaarani A. & Noor Hisham M.Z.A. 2020: Zingiberaceae diversity in Ulu Sat Forest Reserve, Kelantan. In Abdullah M.R.C., Abong N.N.D., Jemali N.J.N., Amaludin N.A. & Nordin S.M. (eds): Ulu Sat Forest: The Heart of Kelantan's Nature Conservation. Forestry Department of Kelantan, Malaysia, pp. 72-78.
    48. Jia X.-C., Li J., Lu G.-H. & Wang Y.-Q. 2015: The concrete evidence of flexistyly in Plagiostachys: pollination biology of a wild ginger on Hainan Island, China. - Ecol. Evol. 5: 5364-5371. Go to original source...
    49. Johnson N.F. & Triplehorn C.A. 2005: Borror and DeLong's Introduction to the Study of Insects. 7th ed. Tmonson Brooks/Cole, Belmont, 866 pp.
    50. Jones G.D. & Jones S.D. 2001: The uses of pollen and its implication for entomology. - Neotrop. Entomol. 30: 314-349. Go to original source...
    51. Kamaruddin F. & Zalipah M.N. 2020: Observation of flower visitors to determine their potential role as pollinators of Ixora coccinae and Ruellia simplex. - J. Undergrad. Res. 2: 61-70. Go to original source...
    52. Kato M. 1996: Plant-pollinator interactions in the understory of a lowland mixed dipterocarp forest in Sarawak. - Am. J. Bot. 83: 732-743. Go to original source...
    53. Kato M., Itino T. & Nagamitsu T. 1993: Melittophily and ornithophily of long-tubed flowers in Zingiberaceae and Gesneriaceae in West Sumatra. - Tropics 2: 129-142. Go to original source...
    54. Katumo D.M, Liang H., Ochola A.C., Lv M., Wang Q.-F. & Yang C.-F. 2022: Pollinator diversity benefits natural and agricultural ecosystems, environmental health, and human welfare. - Plant Div. 44: 429-435. Go to original source...
    55. Kaufman S. 2016: Zingiber officinale (Ginger). CABI Compendium. URL: https://www.cabidigitallibrary.org/doi/10.1079/cabicompendium.57537#sec-36
    56. Keys R.N., Buchmann S.L. & Smith S.E. 1995: Pollination effectiveness and pollination efficiency of insects foraging Prosopis velutina in South-eastern Arizona. - J. Appl. Ecol. 32: 519-527. Go to original source...
    57. Kittipanangkul N. & Ngamriabsakul C. 2006: Pollen and pollinator limitation of seed initiation in Etlingera littoralis (J. König) Giseke (Zingiberaceae) in Klong Klai Basin, Khao Nan National Park, Thailand. - Walailak J. Sci. Tech. 3: 207-217.
    58. Klein A.-M., Steffan-Dewenter I. & Tscharntke T. 2003: Bee pollination and fruit set of Coffea arabica and C. canephora (Rubiaceae). - Am. J. Bot. 90: 153-157. Go to original source...
    59. Larsen K. 1996: A preliminary checklist of the Zingiberaceae of Thailand. - Thai Forest Bull. (Bot.) 24: 35-49.
    60. Larsen K., Ibrahim H., Khaw S.H. & Saw L.G. 1999: Gingers of Peninsular Malaysia and Singapore. Natural History Publications, Borneo, 135 pp.
    61. Lefebvre V., Villemant C., Fontaine C. & Daugeron C. 2018: Altitudinal, temporal and trophic partitioning of flower-visitors in Alpine communities. - Sci. Rep. 8: 4706, 12 pp. Go to original source...
    62. Leong-©kornièková J., Thame A. & Chew P.T. 2014: Notes on Singapore native Zingiberales I: A new species of Zingiber and notes on the identities of two further Zingiber taxa. - Gardens' Bull. (Singapore) 66: 153-167.
    63. Li Q.-J., Xu Z.-F., Kress W.J., Xia Y.-M., Zhang L., Deng X.-B., Gao J.-Y. & Bai Z.-L. 2001: Flexible style that encourages outcrossing. - Nature 410: 432. Go to original source...
    64. Ling S.-J., Lu T. & Ren M.-X. 2020: A novel type of mirror-image flowers caused by lateral bending of the floral tube in a bumblebee-pollinated plant. - Flora 272: 151694, 7 pp. Go to original source...
    65. Liu R., Chen D., Luo S., Xu S., Xu H., Shi X. & Zou Y. 2020: Quantifying pollination efficiency of flower-visiting insects and its application in estimating pollination services for common buckwheat. - Agric. Ecosyst. Environ. 301: 107011, 10 pp. Go to original source...
    66. Majestic C.J., Raguso R.A. & Ashman T.-L. 2009: The sweet smell of success: Floral scent affects pollinator attraction and seed fitness in Hesperis matronalis. - Funct. Ecol. 23: 480-487. Go to original source...
    67. Maknoi C., Ruchisansakun S. & Jenjittikul T. 2019: Curcuma putii (Zingiberaceae), a new species from Thailand. - Ann. Bot. Fenn. 56: 351-353. Go to original source...
    68. Maldonado M.B., Lomáscolo S.B. & Vázquez D.P. 2013: The importance of pollinator generalization and abundance for the reproductive success of a generalist plant. - PLoS ONE 8(10): e75482, 6 pp. Go to original source...
    69. Mekuriya W. & Mekibib B. 2018: Review on the medicinal values of ginger for human and animal ailments. - J. Vet. Sci. Technol. 9: 519, 5 pp. Go to original source...
    70. Melati, Palupi E.R. & Bermawie N. 2015: Floral biology of ginger (Zingiber officinale Rosc.). - Int. J. Curr. Res. Biosci. Plant Biol 2: 1-10.
    71. Melidonis C.A. & Peter C.I. 2015: Diurnal pollination, primarily by a single species of rodent, documented in Protea foliosa using modified camera traps. - Sth Afr. J. Bot. 97: 9-15. Go to original source...
    72. Menon A.N. & Dan M. 2009: Chemical composition of essential oils of Globba species from South India. - J. Essen. Oil Res. 21: 59-60. Go to original source...
    73. Moonkaew P., Nopporncharoenkul N., Jenjittikul T. & Umpunjun P. 2020: Cytogenetic and pollen identification of genus Gagnepainia (Zingiberaceae) in Thailand. - Comp. Cytogenet. 14: 11-25. Go to original source...
    74. Nicolson S.W. & Wright G.A. 2017: Plant-pollinator interactions and threats to pollination: perspectives from the flower to the landscape. - Funct. Ecol. 31: 22-25. Go to original source...
    75. Niissalo M.A., Leong-©kornièková J., Khew G.S. & Webb E.L. 2017: Very small relict populations suggest high extinction debt of gingers in primary forest fragments of a tropical city. - Am. J. Bot. 104: 182-189. Go to original source...
    76. Olesen J.M. & Valido A. 2003: Lizards as pollinators and seed dispersers: an island phenomenon. - Trends Ecol. Evol. 18: 177-181. Go to original source...
    77. Ollerton J. 2017: Pollinator diversity: distribution, ecological function, and conservation. - Annu. Rev. Ecol. Evol. Syst. 48: 353-376. Go to original source...
    78. Ollerton J. 2021: Pollinators and Pollination: Nature and Society. Pelagic Publishing, London, 289 pp. Go to original source...
    79. Ollerton J., Johnson S. & Hingston A. 2006: Geographical variation in diversity and specificity of pollination systems. In Ollerton J. & Waser N. (eds): Plant-Pollinator Interactions: From Specialization to Generalization. University of Chicago Press, Chicago, pp. 283-308.
    80. Ollerton J., Winfree R. & Tarrant S. 2011: How many flowering plants are pollinated by animals? - Oikos 120: 321-326. Go to original source...
    81. Ostrowiecka B., Ta³a³aj I., Brzosko E., Jermakowicz E., Mirski P., Kostro-Ambroziak A., Mielczarek L., Lasoñ A., Kupryjanowicz J., Kotowicz J. & Wróblewska A. 2019: Pollinators and visitors of the generalized food-deceptive orchid Dactylorhiza majalis in North-Eastern Poland. - Biologia 74: 1247-1257. Go to original source...
    82. Pattemore D.E. 2017: Pollination. In Thomas B., Murray B.G. & Murphy D.J. (eds): Encyclopedia of Applied Plant Sciences. Academic Press, Oxford, pp. 309-320. Go to original source...
    83. Paudel B.R., Shrestha M., Dyer A.G. & Li Q.-J. 2017: Ginger and the beetle: Evidence of primitive pollination system in a Himalayan endemic alpine ginger (Roscoea alpina, Zingiberaceae). - PLoS ONE 12(7): e0180460, 18 pp. Go to original source...
    84. Paulus H.F. 2018: Pollinators as isolation mechanisms: field observations and field experiments regarding specificity of pollinator attraction in the genus Ophrys (Orchidaceae and Insecta, Hymenoptera, Apoidea). - Entomol. Gen. 37: 261-316. Go to original source...
    85. Paulus H.F. & Gack C. 1990: Pollinators as prepollinating isolation factors: evolution and speciation in Ophrys (Orchidaceae). - Isr. J. Plant Sci. 39: 43-79.
    86. Pereira A.M. & Coimbra S. 2020: Corrigendum to: Advances in plant reproduction: from gametes to seeds. - J. Exp. Bot. 71: 6697. Go to original source...
    87. Pettersson M.W. 1991: Pollination by a guild of fluctuating moth populations: Option for unspecialization in Silene vulgaris. - J. Ecol. 79: 591-604. Go to original source...
    88. Phillips R.D., Peakall R., van der Niet T. & Johnson S.D. 2020: Niche perspectives on plant-pollinator interactions. -Trends Plant Sci. 25: 779-793. Go to original source...
    89. Rader R., Bartomeus I., Garibaldi L.A., Garratt M.P.D., Howlett B.G., Winfree R., Cunningham S.A., Mayfield M.M., Arthur A.D. & Andersson G.K.S. 2016: Non-bee insects are important contributors to global crop pollination. - Proc. Natn. Acad. Sci. 113: 146-151. Go to original source...
    90. Rader R., Howlett B.G., Cunningham S.A., Westcott D.A. & Edwards W. 2011: Spatial and temporal variation in pollinator effectiveness: do unmanaged insects provide consistent pollination services to mass flowering crops? - J. Appl. Ecol. 49: 126-134. Go to original source...
    91. Reddi C.S. & Bai G.M. 1984: Butterflies and pollination biology. - Proc. Anim. Sci. 93: 391-396. Go to original source...
    92. Rezende K.M., dos Santos R., da Silva A., da Silva P.C., Cordeiro M.H.M. & Silva C.A. 2021: Aspects of the reproductive biology of Zingiber spectabile (Zingiberaceae). - Physiol. Morphol. Appl. Agric. 68: 96-104. Go to original source...
    93. Saensouk P., Theerakulpisut P., Thammathaworn A, Saensouk S., Maknoi C. & Kohkaew P. 2015: Pollen morphology of the genus Curcuma (Zingiberaceae) in Northeastern Thailand. - ScienceAsia 41: 87-92. Go to original source...
    94. Sáez A., Negri P., Viel M. & Aizen M.A. 2019: Pollination efficiency of artificial and bee pollination practices in kiwifruit. - Scientia Horticult. 246: 1017-1021. Go to original source...
    95. Sakai S. & Nagamasu H. 1998: Systematic studies of Bornean Zingiberaceae I. Amomum in Lambir Hills, Sarawak. - Edinburgh J. Bot. 55: 45-64. Go to original source...
    96. Sakai S., Kato M. & Inoue T. 1999: Three pollination guilds and variation in floral characteristics of Bornean gingers (Zingiberaceae and Costaceae). - Am. J. Bot. 86: 646-658. Go to original source...
    97. Sangvirotjanapat S., Hữu Ðãng T. & Newman M. 2020: Ten new species of Globba section Globba from continental South-East Asia. - Thai Forest Bull. (Bot.) 48: 212-233. Go to original source...
    98. Saturni F.T., Jaffé R. & Metzger J.P. 2016: Landscape structure influences bee community and coffee pollination at different spatial scales. - Agricult. Ecosyst. Environ. 235: 1-12. Go to original source...
    99. Schemske D.W. & Horvitz C.C. 1984: Variation among floral visitors in pollination ability: A precondition for mutualism specialization. - Science 225: 519-521. Go to original source...
    100. Simpson B.B. & Neff J.L. 1981: Floral rewards: Alternatives to pollen and nectar. - Ann. Missouri Bot. Garden 68: 301-322. Go to original source...
    101. Singer R.B. & Sazima M. 2001: Flower morphology and pollination mechanism in three sympatric goodyerinae orchids from Southeastern Brazil. - Ann. Bot. 88: 989-997. Go to original source...
    102. Solomon Raju A.J., Suvarna Raju P. & Venkata Ramana K. 2014: Melittophily and malacophily in Ipomoea pes-caprae (Convolvulaceae). - Taprobanica 6: 90-99. Go to original source...
    103. Spira T. 2001: Plant-pollinator interactions: A threatened mutualism with implications for the ecology and management of rare plants. - Nature Areas J. 21: 78-88.
    104. Stavert J.R., Bailey C., Kirkland L. & Rader R. 2020: Pollen tube growth from multiple pollinator visits more accurately quantifies pollinator performance and plant reproduction. - Sci. Rep. 10: 16958, 10 pp. Go to original source...
    105. Stork N.E. 2018: How many species of insects and other terrestrial arthropods are there on Earth? - Annu. Rev. Entomol. 63: 31-45. Go to original source...
    106. Struwe L. 2016: Field Identification of the 50 Most Common Plant Families in Temperate Regions (Including Agricultural, Horticultural, and Wild Species). Rutgers University, New Brunswick, NJ, 60 pp.
    107. Su Q., Qi L., Zhang W., Yun Y., Zhao Y. & Peng Y. 2020: Biodiversity survey of flower-visiting spiders based on literature review and field study. - Environ. Entomol. 49: 673-682. Go to original source...
    108. Syamsuardi, Mansyurdin, Nurainas & Susanti T. 2010: Variasi morfologi polen genus Globba (Zingiberaceae) di Sumatra Barat. - Berkala Penelitian Hayati 16: 89-94. Go to original source...
    109. Takano A., Gisil J., Yusoff M. & Tachi T. 2005: Floral and pollinator behaviour of flexistylous Bornean ginger, Alpinia nieuwenhuizii (Zingiberaceae). - Plant Syst. Evol. 252: 167-173. Go to original source...
    110. Tanaka N., Uehara K. & Murata J. 2004: Correlation between pollen morphology and pollination mechanisms in the Hydrocharitaceae. - J. Plant Res. 117: 265-276. Go to original source...
    111. Tandon V., Kumar A., Rana C. & Rana A. 2016: Pollination - its type, threats and role in environment conservation. - Int. J. Curr. Res. 8: 35744-35751.
    112. Theilade I. 1999: A synopsis of the genus Zingiber (Zingiberaceae) in Thailand. - Nordic J. Bot. 19: 389-410. Go to original source...
    113. Thomas G.E., Geetha K.A., Augustine L., Mamiyil S. & Thomas G. 2016: Analyses between reproductive behavior, genetic diversity and pythium responsiveness in Zingiber spp. reveal an adaptive significance for hemiclonality. - Front. Plant Sci. 7: 1913, 13 pp. Go to original source...
    114. Thompson J.D. 2001: How do visitation patterns vary among pollinators in relation to floral display and floral design in a generalist pollination system? - Oecologia 126: 386-394. Go to original source...
    115. van der Niet T., Jürgens A. & Johnson S.D. 2010: Pollinators, floral morphology and scent chemistry in the Southern African orchid genus Schizochilus. - Sth Afr. J. Bot. 76: 726-738. Go to original source...
    116. Wang G., Chen J., Li Z.-B., Zhang F.-P. & Yang D.-R. 2014: Has pollination mode shaped the evolution of Ficus pollen? - PLoS ONE 9(1): e86231, 7 pp. Go to original source...
    117. Warren S., Harper K. & Booth G. 1988: Elevational distribution of insect pollinators. - Am. Midland Nat. 120: 325-330. Go to original source...
    118. Weiblen G.D. 2002: How to be a fig wasp. - Annu. Rev. Entomol. 47: 299-330. Go to original source...
    119. Whitehead M.R. & Peakall R. 2009: Integrating floral scent, pollination ecology and population genetics. - Funct. Ecol. 23: 863-874. Go to original source...
    120. Wilcock C. & Neiland R. 2002: Pollination failure in plants: why it happens and when it matters. - Trends Plant Sci. 7: 270-277. Go to original source...
    121. Wilson E.O. 1992: The Diversity of Life. Harvard University Press, 424 pp.
    122. Wojcik V. 2021: Pollinators: Their evolution, ecology, management, and conservation. Arthropods. In Ranz R.E.R. (ed.): Arthropods - Are they Beneficial for Mankind? IntechOpen, 22 pp Go to original source...
    123. Wolfe L. & Sowell D. 2006: Do pollination syndromes partition the pollinator community? A test using four sympatric morning glory species. - Int. J. Plant Sci. 167: 1169-1175. Go to original source...
    124. Wright G.A. & Schiestl F.P. 2009: The evolution of floral scent: the influence of olfactory learning by insect pollinators on the honest signalling of floral rewards. - Funct. Ecol. 23: 841-851. Go to original source...
    125. Xu Z. & Chang L. 2017: Zingiberaceae. In Xu Z. & Chang L. (eds): Identification and Control of Common Weeds. Vol. 3. Springer, Singapore, pp. 909-911. Go to original source...
    126. Yue Y., Yu R. & Fan Y. 2014: Characterization of two monoterpene synthases involved in floral scent formation in Hedychium coronarium. - Planta 240: 745-762. Go to original source...
    127. Zahara M., Hasanah M. & Zalianda R. 2018: Identification of Zingiberaceae as medicinal plants in Gunung Cut Village, Aceh Barat Daya, Indonesia. - J. Trop. Horticult. 1: 24-28. Go to original source...
    128. Zhang L., Li Q.-J., Deng X.-B., Ren P.-Y. & Gao J.-Y. 2003: Reproductive biology of Alpinia blepharocalyx (Zingiberaceae): another example of flexistyly. - Plant Syst. Evol. 241: 67-76. Go to original source...
    129. Zhang Z.-Q., Kress W.J., Xie W.-J., Ren P.-Y., Gao J.-Y. & Li Q.-J. 2010: Reproductive biology of two Himalayan alpine gingers (Roscoea spp., Zingiberaceae) in China: pollination syndrome and compensatory floral mechanisms. - Plant Biol. 13: 582-589. Go to original source...
    130. Zhang Y.-W., Zhao J.-M. & Inouye D.W. 2013: Nectar thieves influence reproductive fitness by altering behaviour of nectar robbers and legitimate pollinators in Corydalis ambigua (Fumariaceae). - J. Ecol. 102: 229-237. Go to original source...
    131. Zhou Y., Abbas F., Wang Z., Yu Y., Yue Y., Li X., Yu R. & Fan Y. 2021: HS-SPME-GC-MS and electronic nose reveal differences in the volatile profiles of Hedychium flowers. - Molecules 26: 5425, 15 pp. Go to original source...
    132. Zito P., Rosselli S., Bruno M., Maggio A. & Sajeva M. 2019: Floral scent in a sexually deceptive Ophrys orchid: from headspace collections to solvent extractions. - Plant Signal. Behav. 14: 1552056, 6 pp. Go to original source...

    This is an open access article distributed under the terms of the Creative Commons Attribution 4.0 International License (CC BY 4.0), which permits use, distribution, and reproduction in any medium, provided the original publication is properly cited. No use, distribution or reproduction is permitted which does not comply with these terms.


    Return to the content